Journal of Neurophysiology, Vol 62, Issue 5 1189-1200, Copyright © 1989 by APS
Role of competition among sensory neurons in regulation of pattern of innervation at their central and peripheral targets
B. Mendelson and E. Frank
Department of Neurobiology, Anatomy, and Cell Science, University of Pittsburgh School of Medicine, Pennsylvania 15261.
1. The importance of competitive interactions among muscle sensory
afferents on their projections to central and peripheral targets was
studied by producing large reductions in the number of afferents during
development. Removal of the brachial dorsal root ganglion (DRG2), which
normally supplies the entire sensory innervation of the forelimb, in
bullfrog (Rana catesbeiana) tadpoles caused a smaller number of neurons in
the adjacent thoracic ganglion (DRG3) to sprout into the forelimb and into
the brachial spinal cord. 2. Horseradish peroxidase labeling in
postmetamorphic animals showed that DRG3 neurons innervating the triceps
muscle arborize in a novel but now appropriate area of the spinal cord, the
region containing motoneuronal dendrites. These foreign afferents do not
arborize in inappropriate regions of the spinal gray matter, and their
collaterals have the same rostrocaudal distribution as those of normal DRG2
muscle afferents. 3. After metamorphosis, the number of DRG3 sensory axons
in individual triceps muscle nerves was determined. Normally, two-thirds of
all triceps afferents project to the medial head alone, even though each of
the three heads is of similar size and is contacted by similar numbers of
motoneurons. After DRG2 removal, although the total number of DRG3
afferents projecting to the triceps muscle was smaller than normal, the
medial head still received approximately two-thirds of the axons, just as
in normal frogs. These results suggest that the proportional sensory
innervation of the triceps muscle-heads is not dependent on competitive
interactions among afferents. 4. DRG3 afferents projecting to the forelimb
also sprouted to innervate appropriate brachial motoneurons. The average
strength of connection between individual sensory and motor neurons was
found to be the same as in normal animals, even though there was presumably
more central target space available for each afferent axon. This suggests
that the number and/or strength of central connections made by individual
fibers may be an intrinsic property of muscle sensory neurons.
